Perturbation-based mapping of natural frequencies with direct intracranial stimulation of the human brain

Abstract

Theoretical and experimental evidence suggest that the induction of oscillatory activity by an external rhythmic source on a specific brain area is maximally efficient if the input pattern matches its so-called 'natural' frequency, defined as the predominant neural rhythm at which the activity of this area tends to fluctuate spontaneously. Based on this principle, single pulse Transcranial Magnetic Stimulation (TMS) coupled to scalp electroencephalography (EEG) has provided evidence of frequency-specific power increases within a unique 'natural' frequency band, considered common to the whole lobe.In an attempt to gain deeper insight into this phenomenon and set the basis for a finergrained atlas of 'natural' frequencies, here we analyzed intracranial EEG (iEEG) signals modulated by single pulses of direct electrical brain stimulation in human patients implanted with depth multielectrodes. Our analyses revealed changes in local EEG activity emerging from local oscillators and contributing to a complex distribution of frequency-specific 'natural' rhythmic responses throughout cortical regions. Moreover, challenging the notion of 'natural' oscillations featuring a predominant frequency band characteristic for an entire lobe, our data support a rich diversity of spectral fingerprints (narrowband, vs. broadband or multiband) with single or multiple frequency peaks, often encompassing contiguous frequency bands, operating at a very local scale.Our findings contribute novel insights on which specific brain areas could be more likely to be synchronized at a given frequencies band and their preferred coupling frequencies, features that could ultimately inform on their structural and functional organization. Our results may also increase our mechanistic understanding of invasive and noninvasive brain stimulation and promote further developments of these approaches for the manipulation of brain oscillations subtending normal and impaired cognition.-3- KEYWORDSLocal synchrony, Rhythmic brain activity, Oscillatory patterns, Natural frequency, Oscillation phase, Intracranial direct brain stimulation, Intracranial electroencephalography, Implanted intracranial multielectrodes, Oscillation-based coding, neuromodulation, oscillatory entrainment, Human cognition of the input matches the frequency of the to-be-entrained oscillators 1 . Such approaches prone that oscillatory entrainment could be most easily achieved by tuning stimulation frequency to the most prominent rhythm operating physiologically on the targeted brain region, hence at the so called 'natural' frequency 13,14 . However, mapping efforts exploring the precise distribution of 'natural' rhythms across brain systems and characterizing local 'natural' spectral fingerprints associated to specific brain sites remain a work in progress.The most common strategy to compile atlases of 'natural' rhythmic patterns in the human brain has consisted in studying the spectral components of resting state neurophysiological signals with high resolution EEG/MEG systems 17 . Nonetheles...

The natural frequencies of the resting human brain: an MEG-based atlas

“…The concept of natural frequency has not extensively been used in the literature. Until now, this concept has almost exclusively been employed to refer to the main frequency evoked by direct electrical/magnetic stimulation of a given brain region (Amengual et al, 2019;Ferrarelli et al, 2012;Rosanova et al, 2009). In this study, we have developed a map of natural frequencies that is highly compatible with the results obtained by direct cortical perturbation, but without interfering with ongoing brain activity.…”

“…These studies have accurately detected natural frequencies within the alpha range in the occipital cortex, low beta-band responses in parietal and perirolandic areas, and high beta-band oscillations in the prefrontal cortex (Ferrarelli et al, 2012;Rosanova et al, 2009). Since TMS stimulation is restricted to few locations, Amengual et al (2019) have recently tried to develop a finer-grained atlas of natural frequencies by applying single pulses of intracranial electrical stimulation while recording iEEG in epileptic patients. Although this is a promising tool, the positioning of electrodes is constrained by clinical criteria for ethical reasons, resulting in some regions being over-sampled (e.g., temporal lobe), while others are under-sampled.…”